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Morphological and Anatomical Features of the Flowers and Fruits during the
Development of Chamissoa altissima (Jacq.) Kunth (Amaranthaceae)

Article in Brazilian Archives of Biology and Technology · December 2010

DOI: 10.1590/S1516-89132010000600019

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 1425

Vol.53, n. 6: pp.1425-1432, November-December 2010 BRAZILIAN ARCHIVES OF

ISSN 1516-8913 Printed in Brazil
BIOLOGY AND TECHNOLOGY
A N I N T E R N A T I O N A L J O U R N A L

Morphological and Anatomical Features of the Flowers and

Fruits during the Development of Chamissoa altissima
(Jacq.) Kunth (Amaranthaceae)
Sayuri de Oliveira Oyama, Luiz Antonio de Souza*, Júnior Cesar Muneratto and Adriana
Lenita Meyer Albiero
Departamento de Biologia; Universidade Estadual de Maringá; Av. Colombo, 5790; 87020-900; Maringá - PR -
Brasil

ABSTRACT

The morphology and structure of the flowers and fruits of Chamissoa altissima (Jacq.) Kunth during the
development were analyzed. The plant material was fixed in FAA 50, embedded in historesin and sectioned
according to standard techniques. The flowers presented tepals with betalain and homogeneous mesophyll;
receptacular nectary; anthers with epidermis, endothecium, one middle layer, and uninucleate tapetum; and
monocarpelar ovary with homogeneous mesophyll. The fruit was a circumscissile capsule, presented the same
number of cellular layers that the ovary, and possessed subendocarpic sclerenchyma. The seed was bitegmic,
exotestal and perispermic.

Key words: Perianth, stamen, gynoecium, pericarp, seed

INTRODUCTION investigations are scarce. In the forest remnants of

Lianas or vines are vascular plants that are rooted
in the ground and maintain their stems in a more
or less erect position by making the use of the
other objects for support. This habit of the growth
has the advantage of enabling the plant to get
better light with a maximum economy of
supporting tissues (Daubenmire, 1974). They are
of minor economic importance in the forestry, but
have great ecological relevance in the forests,
supplying the foods for the animals, aiding in the
stabilization of trees and competing for light and
nutrition or causing the mechanical damages.
The morphological and anatomical studies of
Brazilian lianas usually have restricted to the stem.
Reports about the reproductive organ
the Northwest region of Paraná (less than 1% of
native vegetation) a diversity of liana species
occurs, belonging to different families. Chamissoa
altissima (Jacq.) Kunth is abundant in these forest
remnants in which the reproductive organs still
have not been investigated.
Amaranthaceae that includes Chenopodiaceae,
possesses determinate inflorescences (terminal and
axillary), with flowers bisexual or, less commonly,
unisexual, actinomorphic and monochlamydeous
(Judd et al., 2002; Souza and Lorenzi, 2005). Spjut
(1994) reported cypsela, pyxidium and utricle
fruits for the family. Judd et al. (2002)
distinguished Amaranthaceae fruits as an achene,
utricle, or a circumscissile capsule (pyxis), usually
associated with persistent, fleshy to dry, perianth

*
Author for correspondence: lasouza@uem.br

Braz. Arch. Biol. Technol. v.53 n. 6: pp. 1425-1432, Nov/Dec 2010

1426 Oyama, S. O. et al.
and/or bractlets. Souza and Lorenzi (2005)
reported for Amaranthaceae circumscissile
capsule, achene and more rarely berry or drupe.
Chamissoa H. B. K. presents spikes or panicles
with flowers usually bisexual, fruits with
transversal dehiscence, and arillate seeds (Smith
and Downs, 1972). Barroso et al. (1999)
considered Chamissoa consisting of circumscissile
capsule often associated with persistent bracts,
bractlets and perigon, and endosperm.
The flower, fruit and seed anatomy of
Amaranthaceae/Chenopodiaceae was scarce in the
literature. Singh (1964) presented brief description
of the family. Corner (1976) reported Chamissoa
seeds with funicular aril. Pal et al. (1990) studied
the development and the structure of Amaranthus
hypochaondriacus L. seeds. Prego et al. (1998)
described the seed structure of Chenopodium
quinoa Willd. Ronse-Decraeme et al. (1999)
analyzed the floral development of Pleuropetalum
darwinii Hook. Costea et al. (2001) investigated
the pericarp structure in Amaranthus L. species.
Shepherd et al. (2005) examined the variation in
the morphology, anatomy and histochemistry of
Salicornioideae (Chenopodiaceae) fruits and seeds.
Biological studies of lianas, mainly related to the
reproductive organs, have ecological importance;
they are useful in the control investigations of
these species. In view of this, the main purpose of
this work was to present the available information
on the morphology and anatomy of Chamissoa
altissima flower and fruit during the development.
MATERIALS AND METHODS
The flowers and fruits of different developmental
stages of two specimens of Chamissoa altissima
were collected at the forest remnant of Maringá,
Paraná, Brazil. Voucher materials were deposited
at the UEM Herbarium, collection 11731 HUEM.
The analysis of the flowers and fruits was done
using freshly-collected material or material fixed
in FAA 50 and FPA 50, following the protocol of
Johansen (1940). The fixed material was
embedded in historesin and sectioned (cross- and
longitudinal sections) in a rotation microtome,
according to techniques of Feder and O’Brian
(1968)). The sections were stained in toluidine
Braz. Arch. Biol. Technol. v.53 n. 6: pp. 1425-1432, Nov/Dec 2010
blue (O’Brien et al., 1965). Developing fruits were
analyzed in freehand sections stained in astra blue
and safranin (Kraus and Arduin, 1997). Specific
microchemical tests were done for lipid substances
(Sudan III) (Johansen, 1940), mucilage (methylene
blue) (Costa, 1972), betalain (ammonia vapor)
(Johansen, 1940), starch (iodine-potassium iodide
test) and lignin (phloroglucin test) (Berlyn and
Miksche, 1976).
Micromorphological analysis (Bozzola and Russel,
1992) was done with fixed material. After washing
in 0.1M sodium cacodylate buffer, the samples
were dehydrated in a graded acetone series, critical
point dried with CO2, and then mounted on
aluminum stubbs, gold coated, and subsequently
examined using scanning electron microscopy
(Shimadzu SS-550 Superscan). Illustrations were
prepared using a stereomicroscope Willd M3Z
equipped with a reflex camera. Photographs were
taken with the microscope (Olympus BX50, digital
camera Canon Power Shot A95), and subsequently
prepared using the software Zoom Browser EX
4.6. All the samples were prepared on the same
micrometric scale.
RESULTS
Flower
The flowers were bisexual and occurred in panicle,
each flower associated with three bracts (Fig. 1A).
Each flower presented five or six green tepals, five
or six stamens, and a gynoecium with one pistil
(Figs. 1B, C). The pistil consisted of globose
ovary, style, bipartite/tripartite stigma (Figs. 1B,
C), and only one ovule with basal placentation.
The tepals (Figs. 2A, C) presented uniseriate
epidermis with cuticle flange, and periclinal thick-
walled cells in the abaxial face and thin-walled
cells in the adaxial face. There was a hypodermis
with thick-walled cells in the adaxial surface (Fig.
2C). The parenchymatic mesophyll (Fig. 2C) was
homogeneous and chlorophyllaceous, with one to
four cell layers. In the tepal margin and apex, there
was no mesophyll. The vascularization was made
by the largest vein (midrib) from which smaller
veins branched. In the midrib, there was a single
collateral bundle (Fig. 2C). The vascular bundles
showed fibers in the xylem face.
 Morphological and Anatomical Features of the Flowers and Fruits 1427

Figure 1 - Morphology of the Chamissoa altissima flower. A – Inflorescence branch with flowers.
B and C – Flowers in anthesis. (ad = androecium; br = bract; te = tepals) Bars = 3.7cm,
0.6cm, 0.8cm, respectively.

The nectary (Fig. 2A) occurred in the receptacle
and consisted of two regions, one was convex,
globular and close to the base of the ovary and the
other was laminar and remained around the ovary
base. The globular portion (Fig. 2B) possessed
epidermis with modified stomata and nectariferous
tissue with polyhedral cells and relatively richer in
protoplasma. The laminar portion (Fig. 2B)
presented epidermis with slightly elongated and
papillose cells and two to four layers of
parenchymatous cells. The vascularization of the
nectary consisted only of phloem. The anther was
tetrasporangiate. The immature anther wall (Fig.
2D) was constituted by a uniseriate epidermis with
tabular cells, endothecium, one middle layer and
secretory tapetum with uninucleate cells. The
filament presented papillose epidermis,
parenchyma, and one collateral vascular bundle.
The ovary wall (Figs. 2A, 4A) was composed of
uniseriate outer and inner epidermis and
parenchymatous mesophyll with three or four
cellular layers. The vascularization was done by
two collateral bundles. The style (Fig. 2F) had
lenticular shape and presented a single epidermis,
parenchyma, two collateral vascular bundles and
central transmitting tissue. The style was hollow in
the distal portion and presented a solid nature in
the base. The stigma (Fig. 2E) possessed secretory
epidermis with unicellular hairs.
The ovule (Figs. 5A,B) was campylotropous,
bitegmic, crassinucellate and had a long funiculus.
Only the inner integument took part in the
formation of the micropyle (Fig. 5B). The outer
integument (Fig. 5B) was biseriate with the outer
layer composed of radially elongated cells mainly
close to the micropyle. The inner integument (Fig.
5B) was also bi-layered, but a third layer in the
apex could be present. The nucellus was
parenchymatous. It was formed aril in the ovule of
funicular origin, still in pre-anthesis stage.

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1428 Oyama, S. O. et al.

Figure 2 - Flower structure of Chamissoa altissima. A – Flower in longitudinal section. B – Detail

of the globular and laminar portions of the nectary. C – Detail of the tepal in cross-
section. D – Anther in cross-section. E – Stigma in longitudinal section. F – Style in
cross-section. (be = abaxial epidermis; de = adaxial epidermis; ep = epidermis; et =
endothecium; hy = hypodermis; ml = middle layer; ne = nectary; ov = ovary; st =
stamen; ta = tapetum; te = tepal; tt = transmitting tissue; vb = vascular bundle) Bars =
50µm (A,B,C,D,F), 20µm (E).

Fruit and seed
The fruit was usually associated with persistent
tepals and style. In the mature fruit, the tepals were
red due to the betalain presence. The fruit was a
circumscissile capsule dehiscing by a lid (Fig. 3).
During the pericarp differentiation, there was
reduced structural alteration and partial
sclerification of the mesocarp (Fig. 4A, B) and the
formation of the abscission tissue (Fig. 4C) was
observed.
The mature pericarp (Fig. 4B) presented glabrous
epidermal epicarp with tangentially elongated
cells. The mesocarp consisted of parenchyma and
sclerenchyma. The sclerenchymatic mesocarp was
composed of one to three layers of sclereids which
presented thick and sinuous cell walls with simple
pits. The endocarp was represented by the inner
epidermis and consisted of large cells with thin-
walled which could break up easily (Fig. 4B). The
abscission tissue was loose and it was constituted
of thin-walled cells.

Braz. Arch. Biol. Technol. v.53 n. 6: pp. 1425-1432, Nov/Dec 2010

 Morphological and Anatomical Features of the Flowers and Fruits 1429

Figure 3 – Fruit and seed morphology of Chamissoa altissima. A, B – Young fruits. C – Seed
sectioned longitudinally. D – Mature fruit. (ar = aril; em = embryo; li = lid; pr =
perisperm; te = tepal). Bars = 0.7mm (A), 1.2mm (B,D), 0.5mm (C).

Figure 4 - Pericarp in developing of Chamissoa altissima. A – Ovary in cross-section. B – Mature

pericarp in cross-section. C – Young pericarp in longitudinal section. (ar = abscission
region; cm = sclerenchymatic mesocarp; en = endocarp; ep = epicarp; ie = inner
epidermis; oe = outer epidermis) Bars = 50µm.

The integuments were not multiplicative. The
exotesta cells (Fig. 5C) underwent shortly radially
elongation and the inner cell layer could undergo
periclinal division in certain regions of the young
seed becoming biseriate. In the outer surface of the
exotesta thick cuticular layer was deposited. In the
biseriate tegmen (Fig. 5C), the inner layer
presented cuboid cells and the outer layer showed
small tabular cells which became crushed.
Endosperm was nuclear. The funicular aril (Fig.
5D) developed as loops of the elongated cells with
large vacuoles and nuclei.
The mature seed (Figs. 3C, D) was lenticular,
black, and it was involved completely by white,
fleshy and wrinkled surface aril. It was bitegmic
and exotestal. The exotesta was composed of short
elongated sclereids with lignified reticulate thick-
walled cells. The exotesta was covered by the

Braz. Arch. Biol. Technol. v.53 n. 6: pp. 1425-1432, Nov/Dec 2010

1430 Oyama, S. O. et al.

cuticle and thick striate cuticular layer. The testa
still consisted of one to three layers of
parenchymatous cells (Fig. 5E). The tegmen (Fig.
5E) possessed one cellular layer, occurring two
strata eventually. The perisperm (Fig. 3C) showed
epidermis with cuticle and parenchyma with
content poorly oily and calcium oxalate crystals.
The embryo (Fig. 3C) was curved with long
hypocotyl-radicle axis and two cotyledons of
different dimensions.

Figure 5 - Ovule and seed structure of Chamissoa altissima. A – Scanning electron micrographs
showing ovule and nectary. B – Detail of micropylar region of the ovule in longitudinal
section. C – Detail of chalazal region of the young seed in longitudinal section. D –
Young seed in longitudinal section. E – Mature seed integuments in cross-section. (ar =
aril; cl = cuticular layer; ct = cuticle; ex = exotesta; fu = funiculus; ii = inner integument;
mi = micropyle; nu = nucellus; ne = nectary; oi = outer integument; ou = ovule; st =
stamen; te = testa; tg = tegmen) Bars = 20µm (B,C,E), 50µm(E).

DISCUSSION considered this species as zoochoric in a forest

The persistent perianth or perigone on the fruit can
develop different functions and/or undergo
structural modifications. In the literature, there are
several examples in which the perianth/perigone
may serve as a protective organ as well as a means
of seed dispersal at fruit maturity, as for instance
in Asteraceae, Boraginanaceae, Verbenaceae and
Nyctaginaceae (Roth, 1977; Souza, 2006, 2008).
In C. altissima, the tepals initially acted as
protective and photosynthetic functions and after
acquiring the red color it should act in the seed
dispersal. In fact, Mikich and Silva (2001)
remnant of the Paraná, Brazil.
The C. altissima floral nectary developed on the
receptacle could be classified as toral nectary, in
agreement with Fahn (1990). According to Fahn
(1990), when the secretory cells are
parenchymatous, nectar is secreted into the
intercellular spaces from which it is exuded via
modified stomata. The C. altissima nectary
seemed to have this secretion and exudation type,
for presenting secretory parenchyma and stomata.
The immature anther wall of C. altissima just
presented a middle layer. In agreement with the
anther wall formation and definitions of the types

Braz. Arch. Biol. Technol. v.53 n. 6: pp. 1425-1432, Nov/Dec 2010

 Morphological and Anatomical Features of the Flowers and Fruits
of walls (Davis, 1966), the anther of this species
could belong to the Monocotyledonous type,
common in Caryophyllanae (Dahlgren, 1991). In
the Monocotyledonous type, periclinal divisions
are suppressed in the outer secondary parietal layer
which develops directly into endothecium, while
the inner layer forms the middle layer and the
tapetum. However, the definitive inclusion of the
C. altissima anther in the Monocotyledonous type
needs ontogenetic study of the anther wall.
The differentiation of the ovary wall in the
pericarp of C. altissima didn’t involve increase of
cellular layers. In this the cell divisions ceased
very early during the fruit development, before
fertilization, unlike drupes, legumes, follicles and
capsules that formed adaxial (ventral) meristem
after the pollinization (Roth, 1977; Souza et al.,
2004; Souza, 2006; Souza et al., 2008). The fruit
differentiation of C. altissima consisted mainly in
cell enlargement of the pericarp, thickening of cell
walls of subendocarpic mesocarp, and formation
of the abscission zone.
The mature pericarp of C. altissima presented
reduced number of cellular layers, 6-7 layered
structure. The Amaranthus species pericarp
showed 2-4 layered structure, consisting of 1-
layered epicarp, 1-2 layered mesocarp and 1-
layered endocarp (Costea et al., 2001). There is not
sclerenchyma in the Amaranthus species mesocarp
as in C. altissima; in the Amaranthus species
occurs the thickening of walls in endocarp cells.
In the literature, the fruit registered for Chamissoa
H. B. K. is classified as pyxidium (or pyxis) or
circumscissile capsule (Smith and Downs, 1972;
Barroso et al., 1999). In fact, C. altissima
presented this fruit type that dehisces by a single
transverse rift. The C. altissima fruit was
structurally similar to the Plantago L. one (Souza,
2006) which showed pericarp with few cell layers,
sclerenchymatous subendocarpic mesocarp and
circumscissile dehiscence. The disappearance of
seed coat cells may occur through their absorption
by the growing endosperm, serving as nutrients, or
by being crushed and obliterated through the
growth of the endosperm and embryo, or through
desiccation when thin-walled (Werker, 1997). In
Amaranthaceae/Chenopodiaceae, the integuments
are reduced generally to the exotesta and the
endotegmen, but with three cuticular layers
(Corner, 1976). In Amaranthus hypochondriacus,
the cells of the inner integument and the inner
epidermis of the outer integument finally
degenerate in a mature seed (Pal et al., 1990). In
Braz. Arch. Biol. Technol. v.53 n. 6: pp. 1425-1432, Nov/Dec 2010
1431
C. altissima, the testa and the endotegmen
remained in the seed coat, degenerating only the
outer layer of the inner integument.
The white aril of C. altissima was funicular and
started its formation in the pre-anthesis ovule. It
occurs typically in the genus (Corner, 1976).
Werker (1997) reported that the aril, usually
colored, was attractive to the group of animals,
which acted as dispersal agents, like orange for
ornitochory and white or yellow for
myrmecochory. According to Kapil et al. (1980)
the aril-like appendages are the types of accessory
seed outgrowths. These most impressed the
botanists and, in fact, brought about the greatest
differences of opinion by their heterogenic shapes,
sizes and ways of development. The authors
considered that the one group of arils which
perhaps could not be accounted for were the true
funicular arils, which originated independently
from the seed coat, and should therefore be treated
as separate category.
Chamissoa altissima presented the general pattern
of Amaranthaceae seed as reported by Singh
(1964) and Corner (1976) as bitegmic and
exotestal seed, persistent inner epidermis in the
tegmen, perisperm and curved embryo. However,
all the embryos of
Amaranthaceae/Chenopodiaceae are not curved.
Shepherd et al. (2005) reported that the peripheral
embryos of the Salicornioideae (Chenopodiaceae)
could further characterized as bent, curved and
straight.
RESUMO
Chamissoa altissima (Jacq.) Kunth ocorre em
remanescentes florestais de Maringá, Paraná,
Brasil e se destaca por seus frutos zoocóricos
envolvidos por sépalas vermelhas. As flores e
frutos em diferentes fases de desenvolvimento são
descritos estruturalmente. O material botânico foi
fixado em FAA 50, emblocado em historresina e
secionado conforme técnicas usuais. As flores
apresentam sépalas com betalaína e mesofilo
homogêneo; nectário receptacular; anteras com
epiderme, endotécio, uma camada média e tapete
uninucleado; e ovário monocarpelar com mesofilo
homogêneo. O fruto é uma cápsula circuncisa,
apresenta o mesmo número de camadas celulares
que o ovário, e possui esclerênquima
subendocárpico. A semente é bitegumentada,
exotestal e perispérmica.
 1432 Oyama, S. O. et al.
ACKNOWLEDGMENTS
We thank CNPq (Conselho Nacional de
Desenvolvimento Científico e Tecnológico, Brasil)
for supporting this work (PIBIC Grant to S. O.
Oyama and Research grant to L. A. Souza). We
also thank Dr. O. A. Guimarães, UFPR, Brazil, for
the species identification.
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Received: May 05, 2009;
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Accepted: June 06, 2010.